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1
Department of Pediatric Radiology, Sophia Children's Hospital, University
Hospital Rotterdam, Dr. Molewaterplein 60, 3015 GJ Rotterdam, The
Netherlands.
2
Department of Pediatric Orthopedic Surgery, Sophia Children's Hospital,
University Hospital Rotterdam, 3015 GJ Rotterdam, The Netherlands.
3
Department of Epidemiology and Biostatistics, Erasmus University, Dr.
Molewaterplein 50, Rotterdam, The Netherlands.
Received May 4, 1999;
accepted after revision October 27, 1999.
Address correspondence to S. G. F. Robben.
Abstract
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SUBJECTS AND METHODS. In a prospective study of 224 hips in 112 patients (mean age, 5 years 11 months), the anterior ascending cervical arteries of the hip were identified with color Doppler sonography. Subsequently, we measured the resistive index (RI) with pulsed Doppler sonography.
RESULTS. In 61% (137/224) of hips, a Doppler signal could be obtained. In asymptomatic hips (n = 64), the mean RI was 0.58. In symptomatic hips, the definitive diagnoses and mean values of RI included transient synovitis (n = 31) and 0.92, Perthes' disease (n = 9) and 0.67, and miscellaneous (n = 5) and 0.68. In 28 symptomatic hips, no definite diagnosis could be determined and the complaints spontaneously disappeared during follow-up (mean RI, 0.57). We found no statistically significant difference in the RI of symptomatic versus asymptomatic hips, except in patients with transient synovitis (p < 0.001). In 11 hips with transient synovitis that were reexamined after 4-6 weeks, the RI returned to normal (0.57). The RI in symptomatic hips showed a positive correlation with the amount of effusion (r = 0.69, p < 0.001). In symptomatic and asymptomatic hips, we found no correlation with age (p = 0.9 and 0.1, respectively).
CONCLUSION. The deep capsular vessels of the hip joint can be evaluated on Doppler sonography in more than 60% of hips. Also, the RI is age independent and correlates with the amount of effusion.
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Arteries have been viewed in vitro with various injection or fixation techniques [1,2,3] and in vivo with selective angiography [5]. The arterial blood supply to the femoral head can also be studied indirectly with isotope scanning [6,7,8,9] or MR imaging [10,11,12]. However, no noninvasive techniques were available for the in vivo real-time evaluation of arterial flow to the femoral head until the introduction of Doppler imaging, including color Doppler sonography, duplex Doppler sonography, and, more recently, power Doppler sonography. A study by Graif et al. [13] used Doppler sonography to examine the medial and lateral circumflex arteries in healthy adults, but these vessels have many muscular branches and do not exclusively supply the femoral head. However, the application of these techniques is promising because continuing technical improvements enable sonographers to view very small vessels [14,15,16]. Because of their small size, children, in particular, may benefit from Doppler sonography techniques [17]. A study by Bearcroft et al. [18] viewed the ascending cervical arteries within the cartilaginous femoral head in neonates.
We evaluated the usefulness of Doppler sonography to depict (in vivo) the small feeding arteries of the femoral head in children, to determine the characteristics of the waveform in healthy hips, and to examine waveform characteristics in diseases that affect the hip joint.
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In 11 hips with transient synovitis (nine patients with unilateral disease and one patient with bilateral disease), Doppler sonography was repeated 4-6 weeks later.
Methods
Sonography was performed, by the same investigator, on an Ultramark 9 HDI
unit (Advanced Technology Laboratories, Bothell, WA) with a high-frequency
broadband 7- to 10-MHz linear array transducer or a 128 XP10 unit (Acuson,
Mountain View, CA) with a 7-MHz linear array transducer. Patients were
examined in the supine position, with their legs extended and slightly
externally rotated. Both hips were examined with sonography in a plane
parallel to that of the femoral neck because the anterior capsule of the hip
is best viewed in that plane.
In patients with unilateral symptoms, a pathologic amount of joint effusion was diagnosed if sonography revealed a thickening of the anterior joint capsule of more than 2 mm compared with that in the asymptomatic hip [8, 19,20,21], in which the thickness of the joint capsule was defined as the distance between the femoral cortex and the fascia of the iliopsoas muscle.
In patients with bilateral symptoms, the thickness of the effusion between the anterior and posterior layers of the capsule was measured [22] and considered abnormal if it exceeded 2 mm.
The posterior layer of the anterior joint capsule was subsequently examined with Doppler sonography to identify the anterior ascending cervical arteries (Fig. 1B). A low-pulse repetition frequency (1.25 kHz) and a wall filter of 50 kHz were used. The color gain was set at a level just below the disappearance of color noise. When no vessels were found with color Doppler sonography, another attempt to identify the vessels was made with power Doppler. Next, a pulsed Doppler examination was performed, placing the Doppler sample over the vessel. The pulse-repetition frequency was then adapted to the amplitude of the waveform. The resistive index (RI), defined as the difference between the peak systolic and end-diastolic flow velocities divided by the peak systolic velocity, was measured at least twice in each vessel.
The Doppler examination was limited to 5 min for each hip. In an attempt to estimate the overall vascularization of the femoral head, the number of vessels that could be identified within the limited time frame was assessed. None of the hips with an effusion was aspirated.
Diagnostic Criteria
Afebrile patients with an irritable hip had transient synovitis if
sonography revealed an abnormal effusion and the symptoms subsided within 4
weeks without specific therapy and remained symptom-free for at least 6 months
thereafter.
Perthes' disease was diagnosed with radiography if the typical changes of avascular necrosis appeared on serial radiographs (i.e., condensation, subchondral fracture, collapse, and eventual fragmentation).
Patients had nonspecific synovitis when effusion was present in the hip joint without the classical presentation of transient synovitis [23] and without clinical or serologic signs of rheumatoid arthritis. The discharge diagnosis in this group of patients was reactive or postinfectious synovitis.
The final clinical diagnosis was established 6 months after presentation by reviewing medical and radiologic records.
Statistical Analysis
For statistical analysis, the Statistical Package for the Social Sciences,
version 7.5 (SPSS, Chicago, IL) was used. The Kruskal-Wallis test was used to
analyze the differences between patient groups. Because the differences
between the symptomatic and asymptomatic hips in each patient group were
roughly normally distributed, a comparison of both hips was performed using a
paired t test; for each patient group, outcomes did not differ
significantly, regardless of whether the measurement on the contralateral side
was available.
The 97.5 percentile was calculated to determine the upper limit of the RI in asymptomatic hips.
For hyperemia, the Wilcoxon's signed rank test was used to compare both hips in each disease group.
The correlation between the RI and age and between the RI and effusion was determined by calculating Spearman's rank correlation coefficient.
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All hips with Perthes' disease (n = 9) were in the initial stage according to a study by Edgren [24].
The miscellaneous group (n = 5) consisted of hips with nonspecific synovitis (n = 3), occult fracture of the tibia in a 1-year-old girl that was diagnosed with conventional radiography, and low-grade osteomyelitis of the distal tibia in a 1-year-old boy that was diagnosed with conventional radiography and clinical findings.
In 47 symptomatic hips, no abnormalities were found on sonography or conventional radiography, and symptoms disappeared without specific therapy and the patients remained symptom-free after 6 months. This group was referred to as the "no pathology" group.
In asymptomatic hips, the mean RI was 0.58 (97.5 percentile = 0.70; 2.5 percentile = 0.45) (Table 1 and Fig. 2) and we found no correlation with age (p = 0.1). In symptomatic hips, we also found no correlation with age (p = 0.9)
In transient synovitis, the RI of the symptomatic hip was significantly higher compared with that of the contralateral healthy hip (p < 0.001) (Figs. 3,4,5A,5B). In the other disease groups, the differences in the RI between symptomatic and asymptomatic hips were insignificant. The RI of the symptomatic hips in transient synovitis was significantly higher than that in other disease groups, which showed no mutual differences.
We determined a linear correlation between the RI and the amount of effusion (r = 0.73; p <0.001) (Fig. 6).
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Patients with an abnormal effusion (n = 37) were divided into two
groups: patients with a normal RI (<0.70) and those with an increased RI
(
0.70). The distribution of diseases is summarized in
Table 2.
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In 11 hips with transient synovitis, examination was repeated after 4-6 weeks. On the repeated examination, the patients were symptom-free, their effusions had disappeared, and their RI values had returned to normal (0.57; SD = 0.07) (Fig. 5A,5B).
The mean number of vessels that could be identified in each hip was one (range, 0-3 vessels). No significant differences could be found, either between symptomatic and asymptomatic hips in all groups, or between groups mutually.
No vessels could be identified in 87 hips, either with color (or power) or with duplex Doppler sonography; in 20 hips, accurate Doppler measurements were impossible because of agitation (mean patient age, 3 years 2 months). The other patients (67 hips) in whom no signal could be obtained had a mean age of 7 years 10 months (SD, 3 years 7 months; range, 1-15 years). This is significantly older than the patients in whom a Doppler signal could be detected (mean age, 5 years 5 months, p < 0.001).
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It was more difficult to obtain Doppler signals in older children than in younger children. This difficulty can be attributed to geometric factors, such as the increasing distance between the transducer and the femoral neck in older children and the progressive reduction of the number of vessels with age [1].
A recent sonographic study on the vascularity of the femoral head [18] examined the intrinsic vessels within the cartilaginous femoral head in neonates, but this method fails in older children because of the progressive ossification of the cartilaginous structures. The method used in this study enables the visualization of the arterial supply to the femoral head after the onset of epiphyseal ossification.
Asymptomatic Hips
In asymptomatic hips, the duplex Doppler waveform resembles a
low-resistance vascular bed with a mean RI of 0.58, which was fairly constant.
The 97.5 percentile was 0.7 and considered the upper limit of normal. In this
context, it is important to identify the posterior layer of the anterior joint
capsule because vessels in the anterior layer
(Fig. 1B) characteristically
show a high resistive type waveform (Fig.
7) and do not contribute to the blood supply of the femoral head.
Especially in hips without effusion, special attention must be paid to
correctly identify the posterior layer.
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Symptomatic Hips
In this study, the RI in hips with transient synovitis was significantly
higher than that of other disease groups. The RI in other disease groups did
not show mutually significant differences. The difference between transient
synovitis and other diseases can be explained by a relatively large effusion
in patients with transient synovitis (Table
1). In fact, it is probable that effusion is the sole cause of the
increase of the RI for three reasons. First, we noted a linear correlation
between RI and the amount of effusion (r = 0.73, p <
0.001) (Fig. 6), and increasing
amounts of effusion cause a progressive decrease of diastolic velocity,
resulting in the arrest in diastolic flow (I = 1) and, eventually, a
reversal of diastolic flow (I > 1) (Figs.
3,
4, and
5A). Second, RI values returned
to normal when the effusion had disappeared in patients with healed transient
synovitis; and third, virtually all symptomatic hips without effusion had a
normal RI, regardless of underlying disease.
We considered distention of the capsule to represent the volume of effusion because there is a linear correlation between capsular thickening and the volume of effusion. A capsular distention of more than 2 mm is a threshold value beyond which the RI changes. The RI is constant (mean, 0.58) when the amount of effusion is less than 2 mm; however, if the capsule distention exceeds 2 mm, a positive correlation between the width of the effusion and the RI develops. This finding supports the assumption of many studies suggesting that a distention of the anterior joint capsule of more than 2 mm is the threshold between physiologic and abnormal amounts of effusion [8, 19, 22, 27,28,29,30,31].
Although we noted a linear correlation between the amount of effusion and
the RI, no increase in RI was identified in several patients, despite a large
effusion (Table 2 and
Fig. 6). To evaluate this
finding, we divided hips with an abnormal effusion (>2 mm) into two groups:
group A included patients (n = 26; mean age, 5 years 2 months) with
an increased RI (0.70), and group B included patients (n = 11;
mean age, 6 years 1 month) with a normal RI (<0.70)
(Table 2). The composition of
diseases within both groups differed significantly: group A consisted of only
one hip with Perthes' disease (4%), 24 hips with transient synovitis, and one
hip with nonspecific synovitis, whereas group B consisted of four hips with
Perthes' disease (36%), six hips with transient synovitis, and one hip with
nonspecific synovitis.
Apparently, unlike transient synovitis, a certain amount of effusion does not affect the vascularization of hips with Perthes' disease. An explanation of this finding is that the compliance of the capsule increases because of long-standing effusion (median duration of symptoms was 28 days in Perthes' disease, versus 2 days in transient synovitis), resulting in less pressure per milliliter of effusion [32]. This hypothesis is supported by animal studies that found a decay of intraarticular pressure caused by nonelastic capsular stretching [33]. According to Wingstrand et al. [26], a positive correlation between age and capsular compliance exists, but this does not contribute to the differences between groups A and B because we noted no significant difference in age (p = 0.31).
None of the hip joints with effusion was punctured because none of the patients had clinical signs or symptoms of septic arthritis; therefore, RI values could not be correlated with intraarticular pressure. Although this may be a limitation of our study, we have several reasons supporting our hypothesis that RI values positively correlate with intraarticular pressure. First, RI values show a positive correlation with the amount of effusion. This is analogous to the positive correlation between the amount of effusion and intraarticular pressure, as found by Kallio et al. [25] and Kallio and Ryoppy [32] (r = 0.52). Second, our patients' RI values and intraarticular pressures [26, 34] returned to normal when the effusion disappeared (Fig. 5A,5B). Third, our findings show no correlation between RI and amount of effusion in hips with Perthes' disease. This finding is analogous to the lack of correlation between intracapsular pressure and aspirated volume of fluid in patients with Perthes' disease [35], and it also indicates a correlation between RI and intraarticular pressure.
The mean number of ascending cervical arteries that could be evaluated was one. There were neither statistically significant differences among diseases nor between symptomatic and asymptomatic hips. Therefore, we did not find evidence of hyperemia of the joint capsule in patients with synovitis, a finding that is in accordance with the study of Strouse et al. [36]. These authors made a qualitative evaluation of perfusion by visual comparison of both hips using power Doppler sonography, and found no difference in flow between both hips in children with unilateral transient synovitis. We even found evidence of decreased flow with a mean RI of 0.92. Apparently, power Doppler sonography cannot depict these differences in flow characteristics.
In conclusion, we determined the feasibility of the in vivo evaluation of the vascularization of the femoral head in children. This technique provides a tool for further studies on hemodynamic changes in diseased and healthy hips.
Acknowledgments
We thank Teun Rijsdijk and Andries Zwamborn for preparing our photographs
and illustrations.
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= no pathology, • = Perthes' disease, 
= miscellaneous.